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 Table of Contents  
REVIEW ARTICLE
Year : 2020  |  Volume : 9  |  Issue : 3  |  Page : 231-238

Port-site infection due to nontuberculous mycobacteria following laparoscopic surgery


1 Department of Infectious Diseases and Microbiology, Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, Sydney, Australia
2 Department of Infectious Diseases and Microbiology; Sydney Medical School and the; Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, Sydney, Australia
3 Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, Sydney; Department of Paediactric Surgery, Children's Hospital West Mead, Australia

Date of Submission20-Feb-2020
Date of Decision20-May-2020
Date of Acceptance14-Jun-2020
Date of Web Publication28-Aug-2020

Correspondence Address:
Waniganeththi Arachchige Manori Piyumal Samaranayake
No. 57/17, Railway Station Road, Veyangoda
Australia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmy.ijmy_32_20

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  Abstract 


Nontuberculous mycobacteria (NTM) are commonly found in soil and water and can cause nosocomial infections by contaminating equipment and disinfectants solution used in hospitals. NTM port-site infection after laparoscopic surgery is increasingly observed, but its clinical features, management, and prevention have not been reviewed adequately. We performed a comprehensive literature review of reports that described the clinical manifestation and management of NTM port-site infections following laparoscopic surgery. The perceived increase in NTM port-site infections is likely multifactorial, influenced by greater awareness, better diagnostics, changes in medical practice, increased prevalence of immunosuppression, and potential pathogen spread. Widespread resistance to common disinfectants is a major concern. Patients with NTM port-site infections typically present 1–3 months after the laparoscopic intervention with chronic local and minimal systemic symptoms. Surgical excision plays an important role in localized or refractory cases. Medical treatment should be guided by species identification and in vitro drug-susceptibility testing (DST) of the infecting NTM strain, with a combination of second-line antituberculosis agents, given for a prolonged duration. NTM port site infection is best prevented by meticulous skin preparation and infection control, using only sterilized supplies for laparoscopic surgery.

Keywords: Laparoscopy, nontuberculosis mycobacteria, port-site infection


How to cite this article:
Piyumal Samaranayake WA, Kesson AM, Karpelowsky JS, Outhred AC, Marais BJ. Port-site infection due to nontuberculous mycobacteria following laparoscopic surgery. Int J Mycobacteriol 2020;9:231-8

How to cite this URL:
Piyumal Samaranayake WA, Kesson AM, Karpelowsky JS, Outhred AC, Marais BJ. Port-site infection due to nontuberculous mycobacteria following laparoscopic surgery. Int J Mycobacteriol [serial online] 2020 [cited 2020 Oct 27];9:231-8. Available from: https://www.ijmyco.org/text.asp?2020/9/3/231/293544




  Introduction Top


Nontuberculous mycobacteria (NTM) are environmental opportunistic pathogens that are usually found in the presence of structural lung disease and immunodeficiency with varying degrees of virulence.[1] NTM infections cause a broad range of clinical syndromes including wound or surgical-site infection, lymphadenopathy,[2],[3] pulmonary disease,[4] catheter-site infection,[2] bacteremia with disseminated disease,[5] and nosocomial infections.[2],[6]

Minimally invasive laparoscopic surgery has become the preferred technique for a wide variety of diagnostic and therapeutic procedures in abdominal and pelvic surgery since it is associated with less pain, early ambulation, early discharge, and improved cosmetic outcomes.[7] Port-site infection caused by NTM is an infrequent but well-documented complication that can occur following laparoscopic surgeries resulting in significant morbidity, prolonged hospital stay, and unsightly scarring.[7],[8],[9]

Recent reports suggest that port-site infection due to NTM by direct or indirect contamination at the time of laparoscopic surgery is on the rise.[2],[10],[11] NTM persistence in hospital water systems, relative resistance to disinfectant solutions, persistence in biofilms, and substandard infection control practices make it likely that these species will continue to be a threat in hospital settings. However, the clinical conditions, demographic characteristics, management, outcome, and prevention of port-site infection due to NTM have not been reviewed in detail. We performed a comprehensive literature review of case reports and case series, describing NTM port-site infection following laparoscopic surgery, by searching the MEDLINE, Medline Plus, PubMed, Google Scholar, and the Cochrane Central Register of Controlled Trials (CENTRAL Cochrane Library) database, for all English language articles, using the search terms “port site infection,” “laparoscopy,” and “non-tuberculous,” or “atypical mycobacteria.” Additional studies were identified from the references of identified papers.


  Pathogenesis and Likely Environmental Reservoirs Top


NTM exhibits great variation in growth rates, colonial morphology, and antibiotic and biocide susceptibility.[1],[12],[13] Mycobacteria are broadly classified as slow- or rapid-growing (colony formation in <7 days) based onin vitro growth rates. NTM infection is usually acquired through inhalation or direct contact with water or soil[1],[6] but has also been recognized in health-care-associated infections,[6] due in part to their ability to produce biofilms in aquatic environments leading to persistence in hospital tap water[1],[14],[15],[16] and on medical instruments. Biofilm formation may partially account for the relative resistance of mycobacteria to disinfectants, such as chlorine, organomercurials, alkaline glutaraldehydes, and other commonly used disinfectants. The thick mycolic acid layer and restricted porin expression also contribute to mycobacterial biocide resistance.[6],[17],[18],[19]

The persistence of mycobacteria in chlorinated water supplies[14],[15] coupled with their disinfectant resistance and improved laboratory diagnostics for isolation are all likely to contribute toward more cases of port-site infection reported in the absence of stringent infection control standards.[8],[15],[20],[21],[22],[23] The use of nonsterile surgical devices (e.g., reusable laparoscopes disinfected with 2% glutaraldehyde), reuse of contaminated trocars, and deficiencies in reprocessing surgical devices have been identified as the likely causes of NTM case clusters in Brazil.[16],[24]Mycobacterium chelonae has been isolated from both clinical samples and the water used to rinse laparoscopes in a hospital case cluster in India,[25] but in many cases, the likely reservoir and mode of acquisition remain unclear.[26],[27],[28],[29]

There is no evidence of specific tissue tropism among NTM species. The fact that certain NTM species are commonly found in skin and soft-tissue infections probably reflects direct inoculation as the route of exposure.[20] The potential existence of mycobacterial endospores[8],[9],[27],[28] has been proposed, but there is limited supportive evidence.[30] Medical devices and prostheses can be affected by biofilm formation,[6],[31] but the most common route of acquisition of port-site infections remains to be determined.

With standard laparoscopic surgery, a trochar and cannula is used to pass the laparoscope into the abdominal cavity. The laparoscope itself should never come in contact with the skin or the abdominal wall. Therefore, infections that arise as a result of laparoscope contamination with NTM should involve deep structures rather than the abdominal wall. A similar pattern of deep NTM infection could be expected if NTM contaminates the valves or tubing used to supply insufflation gas.[32] In contrast, if surgical skin preparation is performed using a solution containing live NTM, microbes could contaminate the skin and abdominal wall during the initial incision or trochar insertion.


  Epidemiological Features Top


[Table 1] provides an overview of studies describing the epidemiological features of NTM port-site infections. There is a suggestion that NTM port-site infections are more common among women, especially within the 25–55 years of age group. This may reflect the fact that women in this age group are more likely to undergo laparoscopic procedures than men. Interestingly, identifiable comorbidities were rare, although diabetes[24],[25],[28],[29] and hepatitis B[23] were identified as potential risk factors. NTM infection can involve single or multiple port sites, with the umbilical port being the most frequently affected.[25],[27],[38] The most commonly isolated NTM species include the rapidly growing species Mycobacterium abscessus, M. chelonae, Mycobacterium fortuitum, and Mycobacterium flavescens [Table 1]. Geographical variation in reported cases and mycobacterial species may be linked to environmental conditions such as humidity, water exposure, and substandard infection prevention practices.
Table 1: Overview of studies describing the epidemiological features of nontuberculous mycobacteria port-site infections

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  Incidence of Port Site Infection Top


Most NTM port-site infections have been reported in the past decade, but there is no accurate incidence data. We focus on port-site infections that occurred subsequent to laparoscopic surgery, involving superficial and deep surgical sites.[41] NTM port-site infection usually presents 1–3 months after laparoscopic surgery [Table 1]. Its slow onset can delay diagnosis with failure to recognize it as a surgical complication. Port-site infection frequencies of 1%–8% have been reported depending on the location and type of surgery.[20] Most cases have been described in India, but Wright et al., 2014,[29] reported 18 cases of NTM infection associated with laparoscopic gastric banding in Australia and Baruque Villar et al., 2015,[24] identified 60 patients at a single surgical unit in Brazil.


  Clinical Features Top


[Table 1] summarizes the recorded clinical features, which usually begins with an erythematous swelling associated with mild pain. This is followed by progressive swelling and discoloration that progress to abscesses that can discharge “sterile” pus (culture negative for typical wound pathogens) with chronic sinus formation. Most patients do not have high fever or signs of systemic infection, although some report low-grade fever with surrounding tissue inflammation.[8],[13],[20],[21],[22] Additional nodules and hyperpigmentation of the skin surrounding a sinus may be seen in later stages.[20] Many patients do not respond to initial empiric antibiotics directed at typical wound pathogens.


  Diagnosis Top


It is important to make an accurate diagnosis since the treatment involves prolonged administration of multiple antibiotics with significant toxicity. Diagnosis depends on a combination of a positive mycobacterial culture together with characteristic clinical signs and symptoms. Inflammatory markers are not helpful,[8],[42] but ultrasound and/or computed tomography scan can be useful to assess deep structures and inform decisions regarding surgical excision or drainage. A positive Mantoux test (sometimes only weakly positive) and a negative Mycobacterium tuberculosis interferon-gamma release assay (IGRA) are consistent with NTM infection, although some species (e.g., Mycobacterium marinum) may evoke a positive Mantoux and IGRA reactions.[43]

Tissue or fluid samples obtained by excision or needle aspiration are preferred, given the decreased chances of a positive NTM culture with the limited material and risk of desiccation associated with swabs.[2],[13] Fluorescence microscopy or traditional Ziehl–Neelsen stains can be used to view mycobacteria,[2],[13],[44] but culture and pan-mycobacterial polymerase chain reaction (PCR) tests may be more sensitive. The diagnosis is further supported by compatible histopathological features such as granulomatous inflammation.[8],[45],[46]


  Culture Top


Culture remains the gold standard diagnostic test and also allows mycobacterial speciation and drug-susceptibility testing (DST). Dedicated NTM culture is usually performed using solid egg-based (Lowenstein-Jensen) or agar-based (Middle brook 7H10 and 7H11) media or liquid broth (Middle brook 7H9). Many mycobacteria, especially rapid growers, will grow on a range of standard clinical media including blood agar, provided incubation is extended, and there is no overgrowth of competing flora. For rapid growers, growth on solid media can usually be detected after 2–5 days of incubation. For slow growers, culture on solid media requires 2–8 weeks, whereas liquid systems are more sensitive and faster.[47] The mycobacterial species can be identified by biochemical reactions, PCR or line probe assays, DNA sequencing of 16S or 23S ribosomal RNA, or matrix-assisted laser desorption ionization time-of-flight mass spectrometry.[2],[8],[13]


  Treatment Top


The treatment of NTM disease is different from the treatment of tuberculosis, disease caused by mycobacteria belonging to the M. tuberculosis complex. It is important to assess the clinical significance of NTM isolation, with a full appreciation of the limitations of current diagnostic tests. No controlled clinical trials of different drug treatment regimens have been conducted, and there is debate about the value ofin vitro DST.[2] However, several case studies have documented good treatment outcomes.[48],[49] Phenotypic or genotypic DST of all clinically significant NTM isolates seems warranted for good patient management,[2] but variable DST results have been observed among NTM species in different laboratories.[12],[27],[47]

The Clinical Laboratory Standards Institute (CLSI) approved a broth microdilution method for antimicrobial testing for NTM.[12] Some laboratories use disc-diffusion testing and E tests for screening methods as they may be simpler, but these methods frequently provide inconsistent results.[47] As NTM shows a limited response to isoniazid, rifampicin, pyrazinamide, and ethambutol, DST should include additional drugs such as macrolides, quinolones, oxazolidinones, tetracyclines, and aminoglycosides, as well as broad-spectrum beta-lactam antibiotics. Susceptibility data suggest that several newer antibiotics (bedaquiline, linezolid, telithromycin, and tigecycline) may have activity against NTM,[50],[51],[52] but their role in treatment remains to be defined.

Current American Thoracic Society and Infectious Diseases Society of America (ATS/IDSA) guidelines recommend the use of combination therapy with different classes of agents, as rapidly growing NTM can develop resistance by mutation while on therapy, and inducible macrolide resistance has been demonstrated in M. fortuitum and M. abscessus.[2],[29] It is recommended to use a macrolide (clarithromycin or azithromycin) combined with parenteral medications such as amikacin, cefoxitin, or imipenem for skin and soft-tissue infections caused by Mycobacterium abscesuss, while imipenem is preferred for M. chelonae, as it is uniformly resistant to cefoxitin.[2] The suggested treatment for M. fortuitum infection is combination therapy with at least two active agents as guided by DST results.[2] [Table 2] summarizes the outcomes achieved with different drug regimens. There is no consensus regarding the correct duration of therapy, except that prolonged treatment is required to prevent disease relapse. ATS/IDSA guidelines recommend a minimum of 4 months of therapy with at least two agents within vitro activity. It is important to monitor treatment tolerance and drug toxicity. Poor treatment response may signify drug resistance, nonadherence, or the need for surgical debridement.
Table 2: Outcome and regimens used to treat nontuberculous mycobacteria port-site infections

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  Surgical Debridement Top


Although prolonged treatment with antimicrobial drugs alone can achieve cure in some cases, good outcomes often require extensive debridement and removal of prosthetic material.[28],[37],[53] Subsequent recurrence has been documented with incomplete debridement and failure to remove all prosthetic material.[29] Surgery of minor and superficial infections may leave an unsightly scar and facilitate contiguous NTM spread. International guidelines reserve surgical debridement for cases with extensive tissue necrosis, abscess formation, or poor response to appropriate antimicrobial therapy.[2],[20],[52] The ability of rapidly growing NTM species to form biofilms and adhere to artificial surfaces favors the removal of any medical devices or foreign bodies that are likely to be involved in the infection.[2],[16],[28],[29],[35]


  Prevention Top


It is worth considering why clean wounds get infected with NTM.[54] A breach in sterilization protocol is the most common cause of such an infection.[8],[15],[20],[23],[24],[25],[27] The use of disposable laparoscopic instruments is the gold standard for the prevention of infection. However, these are rarely used in developing countries due to cost restraints. Most laparoscopic instruments are not able to withstand the heat of sterilization by autoclaving. As a result, high-level disinfection using glutaraldehyde is widely used. There is no evidence that glutaraldehyde disinfection increases the risk of NTM infections,[54],[55] but increased resistance to glutaraldehyde has been documented in M. chelonae, M. massiliense, and M. smegmatis.[8],[15],[18],[25]

Failure to completely disassemble and clean the multiple joints and crevices, where blood and tissue can collect in scopes, has been identified as a problem in many countries.[15],[24],[25],[55] Viana-Niero et al., 2008,[56] suggested that inadequate cleaning, combined with suboptimal glutaraldehyde concentrations and equipment contact time, may have contributed to the selection of M. abscessus subsp. bolletii strains resistant to glutaraldehyde. A thorough cleaning followed by high-level disinfection is the minimum required. All laparoscopic instruments must be thoroughly cleaned after use, with the complete dismantling of parts to ensure the removal of all organic material. Minimum instructions must be followed regarding the concentration, contact time, and cycles of use for high-level instrument disinfection using appropriate agents. Plasma sterilizers or ethylene oxide methods have been shown to reduce NTM colonization and infection,[54] but comparisons with glutaraldehyde disinfection have not been done. In addition, water used to rinse the instruments must be sterile. It is important to note that the US Center for Disease Control and Prevention recommends sterilization as the minimum requirement, emphasizing that the risk posed by devices that have not been sterilized cannot be fully eliminated.[54] Sterility of skin preparation solutions should also be ensured. NTM can also contaminate aqueous disinfectant solutions, and most recent guidelines recommend alcohol-based surgical skin preparation.


  Conclusion Top


NTM port-site infection is a frustrating complication of laparoscopic surgery. Stringent cleaning and sterilization of laparoscopic instruments and solutions used to disinfect the skin is essential to prevent infections. Treatment is generally successful but requires prolonged treatment with DST-guided multidrug regimens.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Abstract
Introduction
Pathogenesis and...
Epidemiological ...
Incidence of Por...
Clinical Features
Diagnosis
Culture
Treatment
Surgical Debridement
Prevention
Conclusion
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